Phenotypes optimized for early‐life reproduction exhibit faster somatic deterioration with age, revealing a latent cost of high condition

Abstract

High condition enables individuals to express a phenotype with greater reproductive potential. However, life-history theory predicts that reproduction will trade off with somatic maintenance and viability, and several studies have reported faster age-related decline in performance in high-condition individuals, suggesting that high condition in early life is associated with accelerated somatic deterioration. This trade-off may be especially pronounced in males, which often express condition-dependent secondary sexual traits that can impose viability costs during development and through damage-inflicting adult sexual behaviours. To test this prediction, we reared larvae of the neriid fly Telostylinus angusticollis on diets of varying nutrient content and quantified somatic deterioration in solitary males, males housed in all-male or mixed-sex groups and immobilized males subjected to mechanical stress. We found that males reared on a nutrient-rich larval diet (high-condition males) suffered a higher rate of somatic deterioration with age, particularly when housed in groups. Perhaps as a result of accelerated somatic deterioration, high-condition males did not outlive low-condition males. In addition, high-condition males housed in all-male groups experienced a greater reduction in escape response with age than males housed in mixed-sex groups, suggesting that male-male combat promotes somatic deterioration. However, even when immobilized, high-condition males were still found to be more susceptible to somatic damage than low-condition males. Our findings suggest that a high-condition male phenotype is more prone to somatic damage, both as a result of associated behaviours such as combat, and because of the inherent fragility of the high-condition body.

Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild

“…Other studies have reported similarly complex phenotypic effects of early life environmental quality: rich larval diets can lead to increased reproductive effort and a shortened lifespan [17,20,21], although we observed the opposite effect here. Given the complex influence of early-life conditions reported in this and other studies, it is not surprising that two recent meta-analyses failed to detect consistent silver spoon effects on lifespan or actuarial senescence in laboratory or wild populations [30,31].…”

“…Much of the research on trade-offs between early-and late-life performance has focused on the costs of reproductive investment [15][16][17][18][19]. As future survival is uncertain, individuals with abundant access to resources may allocate highly to early-life performance, leading to more rapid declines with age [17,[20][21][22]. Likewise, but less extensively studied, juvenile growth and development may also influence senescence, and are likely to depend on early-life environmental quality.…”

Ageing with a silver-spoon: A meta-analysis of the effect of developmental environment on senescence

“…If a high‐quality environment during early‐life results in higher rates of early‐life reproduction, then the existence of such trade‐offs leads to a prediction that favorable early environmental conditions should be associated with faster rates of senescent decline in late life. This phenomenon of trade‐offs has recently been demonstrated to occur in lab‐based experiments of arthropods (Adler et al ; Hooper et al ).…”

The influence of early‐life allocation to antlers on male performance during adulthood: Evidence from contrasted populations of a large herbivore

“…A meta‐analysis across birds, spiders, insects and fish revealed that the expression of secondary sexual traits is strongly condition‐dependent as the expression of a given sexual trait (known to predict mating success) is generally positively associated with longevity (Jennions, Møller, & Petrie, ). However, while males in good condition during the early stages of life are able to develop the most conspicuous sexual traits, they may suffer from a higher degree of somatic deterioration compared to males that are in low condition during early life, which can lead to an accelerated rate of ageing (Adler, Telford, & Bonduriansky, ). In line with these results, it has recently been argued that the costly nature of secondary sexual traits should be rooted in the theories currently proposed to explain the evolution of ageing (Hooper, Lethonen, Schwanz, & Bonduriansky, ; Tidière et al., ).…”

“…However, while males in good condition during the early stages of life are able to develop the most conspicuous sexual traits, they may suffer from a higher degree of somatic deterioration compared to males that are in low condition during early life, which can lead to an accelerated rate of ageing (Adler, Telford, & Bonduriansky, 2016).…”